Carbon Reallocation Driven by Aerobic–Anoxic Alternation during Methanotrophic Metabolism

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Abstract
Methanotrophs are of fundamental importance in the global methane cycle and hold promise for the bioconversion of methane into valuable products. This study elucidates the impact of alternating aerobic-anoxic conditions on metabolism of the two phylogenetically distinct groups of methanotrophs: Methylomonas koyamae (type I, γ-proteobacteria) and Methylocystis bryophila (type II, α-proteobacteria). Using batch cultivations with single and repeated oxygen pulses, we demonstrated that cyclic aerobic-anoxic alternation significantly increased the secretion of organic compounds. Notably, acetate secretion by the type II methanotroph M. bryophila was observed for the first time. Genome-scale metabolic modeling and flux balance analysis revealed that acetate secretion serves as an auxiliary ATP-generating pathway for M. bryophila under oxygen limitation. We further uncovered a dynamic mechanism: aerobic phases trigger methane uptake and build up intracellular organic carbon pools, while anoxic phases redirect these pools toward acetate and/or hydrogen release to sustain survival under oxygen limitation. This cyclic regimen effectively channels more methane-derived carbon into extracellular acetate. Our findings underscore that redox conditions critically shape methanotrophic metabolism, influencing both the biological methane cycle and the global climate.
Funding Information
  • Innovationsfonden (2105- 00038B)
  • China Scholarship Council (202106090181)

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